The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts

The activities of unicellular microbes dominate the ecology of the marine environment, but the chemical signals that determine behavioral interactions are poorly known. In particular, chemical signals between microbial predators and prey contribute to food selection or avoidance and to defense, factors that probably affect trophic structure and such large-scale features as algal blooms. Using defense as an example, I consider physical constraints on the transmission of chemical information, and strategies and mechanisms that microbes might use to send chemical signals. Chemical signals in a low Re, viscosity-dominated physical environment are transferred by molecular diffusion and laminar advection, and may be perceived at nanomolar levels or lower. Events that occur on small temporal and physical scales in the "near-field" of prey are likely to play a role in cell-cell interactions. On the basis of cost-benefit optimization and the need for rapid activation, I suggest that microbial defense system strategies might be highly dynamic. These strategies include compartmented and activated reactions, utilizing both pulsed release of dissolved signals and contact-activated signals at the cell surface. Bioluminescence and extrusome discharge are two visible manifestations of rapidly activated microbial defenses that may serve as models for other chemical reactions as yet undetected due to the technical problems of measuring transient chemical gradients around single cells. As an example, I detail an algal dimethylsulfoniopropionate (DMSP) cleavage reaction that appears to deter protozoan feeding and explore it as a possible model for a rapidly activated, short-range chemical defense system. Although the exploration of chemical interactions among planktonic microbes is in its infancy, ecological models from macroorganisms provide useful hints of the complexity likely to be found.     

Climate change and marine plankton

Understanding how climate change will affect the planet is a key issue worldwide. Questions concerning the pace and impacts of climate change are thus central to many ecological and biogeochemical studies, and addressing the consequences of climate change is now high on the list of priorities for funding agencies. Here, we review the interactions between climate change and plankton communities, focusing on systematic changes in plankton community structure, abundance, distribution and phenology over recent decades. We examine the potential socioeconomic impacts of these plankton changes, such as the effects of bottom-up forcing on commercially exploited fish stocks (i.e. plankton as food for fish). We also consider the crucial roles that plankton might have in dictating the future pace of climate change via feedback mechanisms responding to elevated atmospheric CO(2) levels. An important message emerges from this review: ongoing plankton monitoring programmes worldwide will act as sentinels to identify future changes in marine ecosystems.     

Effects of sea surface warming on marine plankton

Ocean warming has been implicated in the observed decline of oceanic phytoplankton biomass. Some studies suggest a physical pathway of warming via stratification and nutrient flux, and others a biological effect on plankton metabolic rates; yet the relative strength and possible interaction of these mechanisms remains unknown. Here, we implement projections from a global circulation model in a mesocosm experiment to examine both mechanisms in a multi‐trophic plankton community. Warming treatments had positive direct effects on phytoplankton biomass, but these were overcompensated by the negative effects of decreased nutrient flux. Zooplankton switched from phytoplankton to grazing on ciliates. These results contrast with previous experiments under nutrient‐replete conditions, where warming indirectly reduced phytoplankton biomass via increased zooplankton grazing. We conclude that the effect of ocean warming on marine plankton depends on the nutrient regime, and provide a mechanistic basis for understanding global change in marine ecosystems.     

Environmental influences on long-term variability in marine plankton

The major patterns of geographical and seasonal variability of the plankton of the north-east Atlantic and the North Sea are described to provide the background to a presentation of the dominant patterns of year-to-year fluctuations in the abundance of the plankton of the area for the period 1948 to 1984. A feature of the variability is a marked similarity both between species and between areas. The main pattern of year-to-year change has the form of a quasi linear downward trend in abundance with, superimposed on this, an element of variability with a periodicity of about three years. There is a complex relationship between the plankton and an estimate of changes in the frequency of westerly weather which can be interpreted in terms of influences acting over limited periods of the seasonal cycle coupled with persistence in the stocks of zooplankton. Relationships between year-to-year variations in the abundance of phytoplankton and zooplankton can be interpreted in terms of a response by the zooplankton to variations in food supply coupled with feed-back to the phytoplankton involving in situ nutrient regeneration.     

The biogeography of marine plankton traits

Changes in marine plankton communities driven by environmental variability impact the marine food web and global biogeochemical cycles of carbon and other elements. To predict and assess these community shifts and their consequences, ecologists are increasingly investigating how the functional traits of plankton determine their relative fitness along environmental and biological gradients. Laboratory, field and modelling studies are adopting this trait‐based approach to map the biogeography of plankton traits that underlies variations in plankton communities. Here, we review progress towards understanding the regulatory roles of several key plankton functional traits, including cell size, N₂‐fixation and mixotrophy among phytoplankton, and body size, ontogeny and feeding behaviour for zooplankton. The trait biogeographical approach sheds light on what structures plankton communities in the current ocean, as well as under climate change scenarios, and also allows for finer resolution of community function because community trait composition determines the rates of significant processes, including carbon export. Although understanding of trait biogeography is growing, uncertainties remain that stem, in part, from the paucity of observations describing plankton functional traits. Thus, in addition to recommending widespread adoption of the trait‐based approach, we advocate for enhanced collection, standardisation and dissemination of plankton functional trait data.     

Prokaryotic and viral diversity patterns in marine plankton

Prokaryotes and viruses play critical roles in marine ecosystems, where they are both highly abundant and active. Although early work on both prokaryotes and viruses revealed little of their diversity, molecular biological approaches now allow us to break apart these black boxes. The most revealing methods have been cloning and sequencing of 16S rRNA genes, community fingerprinting (such as terminal restriction fragment length polymorphism; TRFLP), and fluorescent in situ hybridization. Viral diversity can now be analyzed by pulsed field gel electrophoresis (PFGE) of viral genomes. The present paper summarizes recent advances in bacterial and virus diversity studies, and presents examples of measurements from polar, tropical, and temperate marine waters. Terminal restriction fragment length polymorphism shows that many of the same operationally defined prokaryotic taxa are present in polar and tropical waters, but there are also some unique to each environment. By one measure, a sample from over a Philippine coral reef had about 100 operationally defined taxa, whereas one from the open tropical Atlantic had about 50 and from the icy Weddell Sea, about 60. Pulsed field gel electrophoresis of two depth profiles, to 500 m, from Southern California, measured 2 months apart, shows striking similarities in viral genome length diversity over time, and some distinct differences with depth. The euphotic zone samples had extremely similar apparent diversity, but samples from 150 m and 500 m were different. An obvious next step is to compare the bacterial and viral diversity patterns, because theory tells us they should be related.     

Community structure and function in prokaryotic marine plankton

Molecular biodiversity studies of microbial communities have provided invaluable information on the existence of heretofore unknown organisms and on community composition. Cloning and ‘fingerprinting’ techniques have been used many times to study prokaryote community composition of marine plankton. There are still many opportunities for new discoveries in this area, but the results have also opened new questions about the activities of these organisms and their function, going beyond just listing taxa or counting organisms. Rarely can the broad function be inferred from phylogenetic position alone (e.g. cyanobacteria). The recent discovery of abundant non-cyanobacterial marine phototrophs points to our inability to link phylogenetic position with function in a detailed way. One approach we have found fruitful is to combine fluorescence in situ hybridization with microautoradiography, a technique dubbed STARFISH. A recent application has shown that ubiquitous archaea from the deep sea, phylogenetically related to extreme thermophiles, are active in the uptake of amino acids from ambient (nanomolar) concentrations. This suggests the group is at least partly heterotrophic and able to compete successfully with bacteria for nutrients. Other as-yet uncultivated groups are also amenable to similar studies. This revised version was published online in August 2006 with corrections to the Cover Date.     

Fishing impacts on the marine inorganic carbon cycle

1.  Teleost fish excrete precipitated carbonate and make significant contributions to the marine inorganic carbon cycle at regional and global scales. As total carbonate production is linked to fish size and abundance, fishing is predicted to affect carbonate production by modifying fish abundance and size-structure.
2.  We draw on concepts from physiology, metabolic ecology, life history theory, population dynamics and community ecology to develop, validate and apply analytical tools to assess fishing impacts on carbonate production. Outputs suggest that population and community carbonate production fall rapidly at lower rates of fishing than those used as management targets for sustainable yield.
3.  Theoretical predictions are corroborated by estimated trends in carbonate production by a herring population and a coral reef fish community subject to fishing. Our analytical results build on widely applicable relationships between life history parameters and metabolic rates, and can be generalized to most fished ecosystems.
4.   Synthesis and applications . If the maintenance of chemical processes as well as biological process were adopted as a management objective for fisheries then the methods we have developed can be applied to assess the effects of fishing on carbonate production and to advise on acceptable rates of fishing. Maintenance of this ecosystem service would require lower rates of fishing mortality than those recommended to achieve sustainable yield.     

Reconstructing marine plankton food web interactions using DNA metabarcoding

Knowledge of zooplankton in situ diet is critical for accurate assessment of marine ecosystem function and structure, but due to methodological constraints, there is still a limited understanding of ecological networks in marine ecosystems. Here, we used DNA‐metabarcoding to study trophic interactions, with the aim to unveil the natural diet of zooplankton species under temporal variation of food resources. Several target consumers, including copepods and cladocerans, were investigated by sequencing 16S rRNA and 18S rRNA genes to identify prokaryote and eukaryote potential prey present in their guts. During the spring phytoplankton bloom, we found a dominance of diatom and dinoflagellate trophic links to copepods. During the summer period, zooplankton including cladocerans showed a more diverse diet dominated by cyanobacteria and heterotrophic prey. Our study suggests that copepods present trophic plasticity, changing their natural diet over seasons, and adapting their feeding strategies to the available prey spectrum, with some species being more selective. We did not find a large overlap of prey consumed by copepods and cladocerans, based on prey diversity found in their guts, suggesting that they occupy different roles in the trophic web. This study represents the first molecular approach to investigate several zooplankton–prey associations under seasonal variation, and highlights how, unlike other techniques, the diversity coverage is high when using DNA, allowing the possibility to detect a wide range of trophic interactions in plankton communities.     

海洋浮游生物的生态化学计量学研究进展

生态化学计量学可以简单定义为从分子到生物圈的元素生物学,其跨越了环境和生命的各个层次,是构建从分子到生态系统统一化理论的新思路,是生态科学发展的必然趋势.海洋生物占地球生物圈总生物量的50%,是全球生物地球化学循环的重要组成部分,而浮游生物作为海洋生态系统物质循环和能量流动的重要环节,在海洋生态系统元素循环过程中起着关键作用.但是目前关于海洋浮游生物生态化学计量学的研究较零散和缺乏.因此,本文从限制元素影响海洋浮游生物的生态现象和机理、生化物质对营养限制的响应、营养限制的食物链传递与反馈4方面,对海洋浮游生物化学计量学研究进行综述,分析了该领域当前存在的问题,并对我国海洋浮游生物生态化学计量学研究的发展重点提出了展望.
     

Defining seasonal marine microbial community dynamics

Here we describe, the longest microbial time-series analyzed to date using high-resolution 16S rRNA tag pyrosequencing of samples taken monthly over 6 years at a temperate marine coastal site off Plymouth, UK. Data treatment effected the estimation of community richness over a 6-year period, whereby 8794 operational taxonomic units (OTUs) were identified using single-linkage preclustering and 21 130 OTUs were identified by denoising the data. The Alphaproteobacteria were the most abundant Class, and the most frequently recorded OTUs were members of the Rickettsiales (SAR 11) and Rhodobacteriales. This near-surface ocean bacterial community showed strong repeatable seasonal patterns, which were defined by winter peaks in diversity across all years. Environmental variables explained far more variation in seasonally predictable bacteria than did data on protists or metazoan biomass. Change in day length alone explains >65% of the variance in community diversity. The results suggested that seasonal changes in environmental variables are more important than trophic interactions. Interestingly, microbial association network analysis showed that correlations in abundance were stronger within bacterial taxa rather than between bacteria and eukaryotes, or between bacteria and environmental variables.     

Simulated annual plankton production in the northeastern Pacific Coastal Upwelling Domain

A microcomputer simulation model is presented that describesthe generalized plankton production dynamics, in the surfacemixed layer, of the Juan de Fuca Eddy located on the southwesternBritish Columbia continental shelf. The Juan de Fuca Eddy simulationmodel evaluates how the annual biomass production of diatoms,copepods and euphausiids is forced by plankton feeding interactions,seasonal variability in upwelling, water temperature and solarradiation, and generalized fish predation. The model estimatesannual primary production of 345 g C m^–2 year^–1and secondary production of 19.4 g C m^–2 year^–1for copepods and 6 g C m^–2 year^–1 for euphausiids,during 1985–89; -90% of the annual plankton productionwas generated during the April-October upwelling season. Perturbationsof 22 abiotic and biotic parameters, one at a time by ±10%of nominal values, indicated that oceanic variability (e.g.upwelling rate) most strongly affected primary production. Conversely,zooplankton production was most sensitive to variability inbiological parameters describing zooplankton grazing potentialand growth (e.g. gross growth efficiency). Simulated seasonalbiomass patterns of diatoms, copepods and euphausiids were foundto closely match empirical data. However, euphausiid biomassproduction in the Juan de Fuca Eddy alone was unable to meetthe demands of estimated pelagic fish consumption. Local Eddyeuphausiid populations had to be supplemented, from regionaleuphausiids. by a mechanism that is proposed to be linked tothe seasonal pattern and intensity of positive Ekman transport(upwelling).     

Recovery of plankton from hurricane impacts in a large shallow lake

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Climate shifts the interaction web of a marine plankton community

Climatic effects in the ocean at the community level are poorly described, yet accurate predictions about ecosystem responses to changing environmental conditions rely on understanding biotic responses in a food‐web context to support knowledge about direct biotic responses to the physical environment. Here we conduct time‐series analyses with multivariate autoregressive (MAR) models of marine zooplankton abundance in the Northern California Current from 1996 to 2009 to determine the influence of climate variables on zooplankton community interactions. Autoregressive models showed different community interactions during warm vs. cool ocean climate conditions. Negative ecological interactions among zooplankton groups characterized the major warm phase during the time series, whereas during the major cool phase, ocean transport largely structured zooplankton communities. Local environmental conditions (sea temperature) and large‐scale climate indices (El Niño/Southern Oscillation) were associated with changes in zooplankton abundance across the full time series. Secondary environmental correlates of zooplankton abundance varied with ocean climate phase, with most support during the warm phase for upwelling as a covariate, and most support during the cool phase for salinity. Through simultaneous quantitation of community interactions and environmental covariates, we show that marine zooplankton community structure varies with climate, suggesting that predictions about ecosystem responses to future climate scenarios in the Northern California Current should include potential changes to the base of the pelagic food.     

On the life history of the marine plankton diatomStephanopyxis palmeriana

Summary 1. The cell diameter ofStephanopyxis palmeriana ranges between 19 and 156µ. The pleural structure is considered to be specific for the genus. The interphasic nucleus lies in the discus of the hypovalva.2. The cell size can be manipulated during the vegetative phase through SiO₂-deficiency followed by frustule regeneration.3. Only 19 to 60µ wide cells are capable of forming gametes and auxospores. Differentiation begins after light intensity is suddenly increased from 400 to 4000 Lux, and temperature from 15° to 21° C.4. Only 19 to 90µ wide cells are capable of forming resting spores. These are produced in the presence of phosphate-deficiency; maximum production occurs at 12° C. After correction of the phosphate-deficiency, resting spores germinate.5. Morphologically, the life history (formation of gametes, auxospores, resting spores) conforms essentially with the findings onStephanopyxis turris (v.Stosch &Drebes 1964).6. The most important factors controlling the life cycle are cell size, temperature, light and nutrients. The effects which these factors produce inS. turris are compared with those observed inS. palmeriana.

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Zur Entwicklungsgeschichte der marinen PlanktondiatomeeStephanopyxis palmeriana

Kurzfassung Im Frühjahr 1964 wurde die zentrische PlanktondiatomeeStephanopyxis palmeriana (Grev.)Grunow — eine aus japanischen Gewässern stammende Warmwasserform und unsererS. turris sehr nahe verwandt — in Kultur genommen. Schon nach kurzer Zeit war es möglich, den gesamten Formwechsel dieser Alge in seinen Grundzügen kennenzulernen. Mit Hilfe von Wasserimmersionen konnten in direkter Lebendbeobachtung Zellteilung, Meiosis, Befruchtung und Auxosporenbildung mit ihren metagamen Mitosen sowie die Bildung und Keimung der Dauersporen studiert werden. Morphologisch stimmt der Formwechsel mit dem vonS. turris (v.Stosch &Drebes 1964) überein; in der Abhängigkeit von Umweltfaktoren bestehen jedoch Unterschiede. So werden Dauersporen bei dieser zwischen 19 und 156µ Zellbreite (= Transversaldurchmesser) vegetativ existierenden Alge nur von schmalen, unter 90µ breiten Zellen in Gegenwart von Phosphatmangel (spärlich manchmal auch bei Nitratmangel) differenziert. Eine Temperatur von 12° C wirkt dabei sehr begünstigend. Die Keimung der Dauersporen setzt nach Beseitigung des Phosphatmangels ein. Zur Sexualisierung sind nur unter 60µ breite Zellen fähig; sie findet statt nach sprunghafter Steigerung der Beleuchtungsstärke (von 400 auf 4000 Lux) sowie einer Temperaturerhöhung von 15° auf 21° C. Wegen der Dickschaligkeit bereitet die Änderung der Zellgröße auf künstlichem Wege durch SiO₂-Mangel mit nachfolgender Schalenregeneration einige Schwierigkeiten. Diese Manipulationen sind jedoch notwendig, wenn ein Klon ohne Veränderung seines Idiotypus über die Auxospore für unbegrenzte Dauer zur Verfügung stehen soll.

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The studies were carried out in the Botanical Institute of the University, Marburg.     

High local and global diversity of Flavobacteria in marine plankton

Members of the phylum Bacteroidetes are among the most abundant microbes in coastal marine waters, but it is unclear to which extent the diversity within this phylum is covered by currently available 16S rRNA gene sequence information. We, thus, obtained a comprehensive collection of sequence types affiliated with Bacteroidetes in coastal North Sea surface waters and we compared this local diversity with the available sequences of marine planktonic and other aquatic Bacteroidetes. Approximately 15% of > 600 clones from two libraries (August 2000, June 2001) were related to Bacteroidetes, specifically to the Flavobacteria. Local diversity appeared to be almost exhaustively sampled. However, the diversity of the two libraries virtually did not overlap, indicating a pronounced temporal variability of the planktonic Flavobacteria assemblage. The majority of sequence types represented novel phylogenetic lineages, adding 6-7% to the currently known genera and species of Bacteroidetes in marine waters. Different diversity estimators suggested that so far only approximately half of the global diversity of planktonic marine Bacteroidetes has been described. The data set moreover indicated that cultivation-independent techniques and isolation approaches have recovered almost equally sized and virtually non-overlapping fractions of the currently known diversity within this phylum. Interestingly, only 15% of genera of Bacteroidetes from various aquatic environments appear to occur in more than one habitat type.     

Preservation potential of ancient plankton DNA in Pleistocene marine sediments

Recent studies have shown that ancient plankton DNA can be recovered from Holocene lacustrine and marine sediments, including from species that do not leave diagnostic microscopic fossils in the sediment record. Therefore, the analysis of this so-called fossil plankton DNA is a promising approach for refining paleoecological and paleoenvironmental information. However, further studies are needed to reveal whether DNA of past plankton is preserved beyond the Holocene. Here, we identified past eukaryotic plankton members based on 18S rRNA gene profiling in eastern Mediterranean Holocene and Pleistocene sapropels S1 (~9 ka), S3 (~80 ka), S4 (~105 ka), and S5 (~125 ka). The majority of preserved ~400- to 500-bp-long 18S rDNA fragments of microalgae that were studied in detail (i.e. from haptophyte algae and dinoflagellates) were found in the youngest sapropel S1, whereas their specific lipid biomarkers (long-chain alkenones and dinosterol) were also abundant in sediments deposited between 80 and 124 ka BP. The late-Pleistocene sediments mainly contained eukaryotic DNA of marine fungi and from terrestrial plants, which could have been introduced via the river Nile at the time of deposition and preserved in pollen grains. A parallel analysis of Branched and Isoprenoid Tetraethers (i.e. BIT index) showed that most of the organic matter in the eastern Mediterranean sediment record was of marine (e.g. pelagic) origin. Therefore, the predominance of terrestrial plant DNA over plankton DNA in older sapropels suggests a preferential degradation of marine plankton DNA.     

Advance in the toxic effects of petroleum water accommodated fraction on marine plankton

Recently, the impact of petroleum pollution on marine plankton has been complemented by a great concern. This review summarizes the reports about toxic effects of oil water accommodated fraction (WAF) on marine phytoplankton, zooplankton and early life stage of animal. For the oil WAF, toxicants are mainly composed of the aromatic hydrocarbons, such as the benzene hydrocarbons and polycyclic aromatic hydrocarbons (PAHs) with 2–5 rings. The oil WAF, especially the PAHs, can be accumulated in plankton due to their great lipophilic abilities, and thus elicites various deleterious effects. Toxicological tests show that marine plankton is very sensitive to the petroleum WAF, as the order of median effective/lethal concentration is merely μg/L or mg/L. There are species and developmental stages differences of plankton tolerance to petroleum WAF, and the toxicity of different oil WAF is various. Generally, its toxicity enhances with increasing carbonic chain length and benzene ring number. Many studies on the acute and sub-acute toxic effects of oil WAF have been done, however few researches on its chronic toxic effects has been carried out till now. Besides, most reports focused on the levels from molecule to individual, though very little work of petroleum toxic effects has ever been performed on the marine plankton population or community levels. Therefore, it is necessary to continue these studies in future.